Evolvability of the Cichlid Jaw: New Tools Provide Insights into the Genetic Basis of Phenotypic Integration
- 609 Downloads
Phenotypic integration is a phenomenon that manifests itself as the covariation among traits, and is thought to substantially influence how evolution unfolds, both in terms of rate and direction, which ultimately determines evolvability. To date little is known about how integration may change across an adaptive radiation, nor do we have a way of determining its genetic basis. Here we sought to test the hypotheses that (1) higher magnitudes of integration are associated with a greater degree of eco-morphological divergence, and (2) integration has a tractable genetic basis. To this end, we first evaluated the magnitude of integration at the population level in the lower jaws of two Lake Malawi cichlid species that exhibit different degrees of trophic specialization. We find that the more eco-morphologically divergent species does indeed exhibit a significantly higher magnitude of integration, which is consistent with our first hypothesis. Next, we developed a new statistical approach based on jackknife pseudovalues to produce a quantitative trait representative of inter-individual variation in the magnitude of integration. This metric was successfully applied to map the genetic basis of integration in the lower jaws of F2 hybrids derived from the two parental species that exhibited differences in the magnitude of integration. We detected three QTLs and two epistatic interactions that contribute to variation in integration within the cichlid mandible. We also detected a single QTL for lower jaw shape. None of the single QTLs for integration identified here overlapped with the interval for lower jaw shape, although one of the epistatic loci for integration did overlap with shape QTL. These results underscore a complex relationship between integration and shape, but suggest largely distinct genetic bases for these two traits. In all, our results show that phenotypic integration has a tractable, yet complex, genetic basis and that we now have the tools available to shed new light on the mechanisms that both promote and limit craniofacial diversity.
KeywordsIntegration QTL Evolvability Cichlid Craniofacial
We thank members of the Albertson lab and the Behavior and Morphology reading group at UMass for critical reading and feedback on this manuscript. This work was supported by an NSF grant (CAREER IOS-1054909) to R. C. A.
- Albertson, R. C., Streelman, J. T., Kocher, T. D., & Yelick, P. C. (2005). Integration and evolution of the cichlid mandible: The molecular basis of alternate feeding strategies. Proceedings of the National Academy of Sciences of the United States of America, 102(45), 16287–16292. doi: 10.1073/pnas.0506649102.PubMedCentralPubMedCrossRefGoogle Scholar
- Arends, D., Prins, P., Broman, K., & Jansen, R. (2010). Tutorial-Multiple-QTL Mapping (MQM) Analysis. 1–39. Retrieved from http://rqtl.org/tutorials/MQM-tour.pdf.
- Cooper, W. J., Parsons, K., McIntyre, A., Kern, B., McGee-Moore, A., & Albertson, R. C. (2010). Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within African rift-lakes. PLoS ONE, 5(3), e9551. doi: 10.1371/journal.pone.0009551.PubMedCentralPubMedCrossRefGoogle Scholar
- Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., et al. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36(4), 355–376. doi: 10.1007/s11692-009-9076-5.PubMedCentralPubMedCrossRefGoogle Scholar
- Konings, A. (2001). Malawi cichlids in their natural habitat. El Paso, TX: Cichlid.Google Scholar
- Marroig, G., & Cheverud, J. (2005). Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution, 59(5), 1128–1142. Retrieved from http://onlinelibrary.wiley.com/doi/10.1111/j.0014-3820.2005.tb01049.x/abstract.
- Mayr, E. (1954). Change of genetic environment and evolution. In J. Huxley, A. C. Hardy, & E. B. Ford (Eds.), Evolution as a process (pp. 157–180). London: Allen & Unwin.Google Scholar
- Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.Google Scholar
- Pigliucci, M., & Preston, K. (Eds.). (2004). Phenotypic integration: Studying the ecology and evolution of complex phenotypes. New York: Oxford University Press.Google Scholar
- Ribbink, A. J., Marsh, B. A., Marsh, A. C., Ribbink, A. C., & Sharp, B. J. (1983). A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. South African Journal of Zoology, 18(3), 149–309.Google Scholar
- Rosas-Guerrero, V., Quesada, M., Armbruster, W. S., Pérez-Barrales, R., & Smith, S. D. (2011). Influence of pollination specialization and breeding system on floral integration and phenotypic variation in Ipomoea. Evolution; International Journal of Organic Evolution, 65(2), 350–364. doi: 10.1111/j.1558-5646.2010.01140.x.PubMedCrossRefGoogle Scholar
- Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–1774. Retrieved from http://www.jstor.org/stable/10.2307/2410734.
- Streelman, J. T., Albertson, R. C., & Kocher, T. D. (2007). Variation in body size and trophic morphology within and among genetically differentiated populations of the cichlid fish, Metriaclima zebra, from Lake Malawi. Freshwater Biology, 52, 525–538. doi: 10.1111/j.1365-2427.2006.01720.x.CrossRefGoogle Scholar